210Po Activity and Concentrations of Selected Trace Elements (As, Cd, Cu, Hg, Pb, Zn) in the Muscle Tissue of Tunas Thunnus albacares and Katsuwonus pelamis from the Eastern Pacific

Marine Pollution Bulletin 87 (2014) 98–103

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Marine Pollution Bulletin

journal homepage: www.elsevier .com/locate /marpolbul

210Po, Cd and Pb distribution and biomagnification in the yellowfin tunaThunnus albacares and skipjack tuna Katsuwonus pelamis from theEastern Pacific

http://dx.doi.org/10.1016/j.marpolbul.2014.08.0060025-326X/� 2014 Elsevier Ltd. All rights reserved.

⇑ Corresponding author. Tel.: +52 669 983 8400; fax: +52 669 9847209.E-mail address: [email protected] (J. Ruelas-Inzunza).

J. Ruelas-Inzunza a,⇑, M.F. Soto-Jiménez b, A.C. Ruiz-Fernández b, M. Ramos-Osuna a,b, J. Mones-Saucedo a,F. Páez-Osuna b

a Instituto Tecnológico de Mazatlán, Calle Corsario 1, No. 203, Col. Urías, Mazatlán 82070, Sinaloa, Mexicob Universidad Nacional Autónoma de México/Instituto de Ciencias del Mar y Limnología, Explanada de la Azada s/n, Mazatlán 82040, Sinaloa, Mexico

a r t i c l e i n f o a b s t r a c t

Article history:Available online 22 August 2014

Keywords:210PoCdPbThunnus albacaresKatsuwonus pelamisEastern Pacific

We measured Cd and Pb in the muscle and stomach contents of Thunnus albacares and Katsuwonuspelamis to define the distribution of the elements in the tissues and their degrees of biomagnification.210Po was measured in the livers of both species and compared to the results of similar studies. The trophicposition of the tuna species was determined by N isotope measurements. The average activity of 210Poin the liver ranged from 119 to 157 (Bq kg�1 wet weight) in K. pelamis and T. albacares. The trophic posi-tion of T. albacares (4.60) was higher than that of K. pelamis (3.94). The Cd content of the muscle increasedsignificantly with the trophic position of the tuna. d13C in T. albacares and K. pelamis varied, with values of3.13 and 1.88‰, respectively. The d15N values in yellowfin tuna were higher than in skipjack tuna. Thetrophic position of T. albacares (4.60 ± 0.67) was therefore more elevated than that of K. pelamis(3.94 ± 1.06). Pb was biomagnified in T. albacares (transfer factor = 1.46).

� 2014 Elsevier Ltd. All rights reserved.

1. Introduction

The issue of metal biomagnification in marine ecosystemsremains under debate (Barwick and Maher, 2003). Prior studieshave found that Hg is subjected to bioaccumulation and biomagni-fication (Castilhos and Bidone, 2000; Dietz et al., 2000), but thatbiomagnification is nonexistent for Cd and Pb (Amiard et al.,1980; Szefer, 1991). In marine ecosystems at tropical and subtrop-ical latitudes, information on the occurrence of trace metals alongfood chains remains scarce. For the Eastern Pacific surrounding thewest coast of Mexico, there is some evidence of Cd biomagnifica-tion (Ruelas-Inzunza and Páez-Osuna, 2008), but another studyfound that Cd, Cu, Pb and Zn were not positively transferredthrough the entire food web (Jara-Marini et al., 2009). When sim-ulating a marine trophic chain in the Eastern Pacific, a study foundthat concentrations of Pb did not increase as the metal moved upthrough the food chain (Soto-Jiménez et al., 2011).

Classic studies on the food preferences and trophic levels ofmarine organisms are usually conducted using stomach contentsand direct observation of the predators during feeding; however,such approaches have limitations both because these organisms

feed underwater (Walker and Macko, 1999) and because theirdigestion process (Lesage et al., 2001) makes it difficult to identifythe prey. A wider perspective of trophic relationships can beobtained using stable isotope techniques; d13C is usually employedto establish the origin of a trophic web and to recognize the carbonsources of primary producers (Hobson and Welch, 1992). d15N isusually enriched in predators with respect to the concentrationsin the corresponding prey (Minegawa and Wada, 1984; Abendand Smith, 1997); it is therefore used in ecological studies to tracethe trophic levels of organisms. Studies with stable isotopes of Cand N are useful because they provide integrated information onthe food assimilated rather than only on recent consumption(Lesage et al., 2001). Studies related to the transfer of trace metalsin conjunction with stable isotopes of C and N are useful to definethe degree of trophic transfer of pollutants. In the current study,measurements of 210Po, Cd and Pb and of C and N isotopes wereperformed to assess whether biomagnification occurs in the skip-jack tuna Katsuwonus pelamis and the yellowfin tuna Thunnusalbacares in the Eastern Pacific Ocean.

2. Materials and methods

Tuna specimens were captured by a commercial fleet operatingin the Eastern Pacific at a rate dependent on tuna availability.

J. Ruelas-Inzunza et al. / Marine Pollution Bulletin 87 (2014) 98–103 99

Individuals were collected in three areas: (a) adjacent to the BajaCalifornia Peninsula (NW Mexico), (b) in the Gulf of Tehuantepec(Southern Mexico), and (c) in the offshore waters of the PacificOcean (Fig. 1). Thirty-six skipjack (K. pelamis) specimens andforty-four yellowfin (T. albacares) individuals were collectedbetween March and July of 2008. Fish were identified using illus-trated taxonomic keys (Allen et al., 1995). The total weight, totallength and fork length (from the tip of the snout to the fork ofthe tail) were recorded (Table 1). After each fishing trip, fish dissec-tion was conducted in the processing plant; the liver, muscle tissuefrom the median dorsal part of both sides of each animal, andstomach contents were analyzed. Samples were freeze-dried (Lab-conco Freeze-dry System, FreeZone 6) at 80 � 10�3 mBar and�52 �C for 72 h, followed by manual grinding in an agate mortarwith a pestle. Samples were processed and analyzed in a HEPA(class 1000) filtered air, trace metal clean laboratory, using highpurity reagents and water. For Cd and Pb, acid digestion (J.T. Bakerconcentrated nitric acid, trace metal grade) of duplicate subsam-ples was performed using Teflon vials (Savillex™) at 120 �C for3 h (MESL, 1997). For 210Po, aliquots of 0.3 g of dried tissue spikedwith 209Po as a yield tracer were digested overnight in closed Tef-lon vials (Savillex™) on a hotplate using 10 ml of concentratedHNO3 at 150–180 �C. The residue was converted to a chloride saltby repeated evaporation with 12 M HCl, followed by redissolutionin 0.5 M HCl and 0.2 g of ascorbic acid. Po isotopes were depositedon a silver disc in contact with the acid solution overnight using anorbital shaker at room temperature. Po activity was measured bya-spectrometry using ORTEC silicon surface barrier detectors cou-pled with a PC running Maestro™ data acquisition software. Blankswere run in parallel to correct for any contamination. The resultsare expressed in Bq kg�1 dry weight (dw). For comparative pur-poses, 210Po activities were converted to wet weight (ww) accord-ing to: 210Poww = 210Podw � (100-humidity percentage)/100(Magalhães et al., 2007).

Before running analyses of stable isotopes of C and N in musclesamples, the lipids and carbonates were extracted from the sam-ples using cyclohexane and HCl vapor, respectively. To accomplish

Fig. 1. Collection areas of skipjack tuna Katsuwonus pelamis (filled circles) and ye

this, sub-samples of �100–200 mg of fine powder were agitatedwith 4 ml of cyclohexane for 1 h and then centrifuged for 10 minat 3500 rpm; the supernatant containing the lipids was discarded.Sample were dried overnight in an oven at 60 �C and then treatedwith HCl vapor for 4 h inside a glass desiccator and again driedovernight. Aliquots were weighed, pressed into tin capsules(Costech, Valencia, CA), and sent to the Stable Isotope Facility atthe University of California in Davis for determination of the stableisotope ratios (13C/12C and 15N/14N). Analyses of the stable isotopecompositions of the samples were performed using a PDZ EuropaANCA-GSL elemental analyzer interfaced with a PDZ Europa 20–20 isotope ratio mass spectrometer (Sercon Ltd., Cheshire, UK).The results are reported as parts per thousand (‰) differences froma corresponding standard: dX = [(Rsample/Rstandard) � 1] � 103,where R = 15N/14N or 13C/12C. The final delta values were expressedrelative to international standards V-PDB (Vienna PeeDee Belem-nite) and Air for carbon and nitrogen, respectively. At least two dif-ferent laboratory standards, calibrated against NIST StandardReference Materials and compositionally similar to the samples,were analyzed with the sample batches. The long-term standarddeviation was 0.2‰ for 13C and 0.3‰ for 15N.

Cd and Pb were measured by graphite furnace atomic absorp-tion spectrophotometry (Varian SpectrAA220); blanks wereincluded with every batch of samples. The quality of the analyticalmethod was assessed by trace metal determinations of certifiedmaterial consisting of fish protein (DORM-3) and shark liver(DOLT-4) in parallel with the samples. Measured concentrationsin reference materials were within certified intervals (mean per-centage recoveries were 103 in the case of Pb and 101 for Cd).Trace metal concentrations were expressed as lg g�1 dry weight.Conversions of metal concentrations from dry weight (d.w.) towet weight (w.w.) were performed according to the water contentof the tissue of interest. Significant differences in metal concentra-tions between species were defined using Student’s t-test. Biomet-ric variables (weight, total length and fork length) were correlatedwith d15N. Statistical analyses were performed using Graph-Pad Prism 4.0 (Graph Pad Software, San Diego, CA). Average

llowfin tuna Thunnus albacares (filled squares) in the Eastern Pacific Ocean.

Table 1Biological information and mean concentrations (lg g�1 dry weight) of Cd and Pb in muscle and stomach content and transfer factor in K. pelamis and T. albacares from the EasternPacific.

Species Common name N Weight (kg) ± SD Total length (cm) ± SD Fork length (cm) ± SD Element Muscle Stomach contenta Transfer factor

K. pelamis Skipjack tuna 36 3.1 ± 1.4 55.4 ± 7.6 51.6 ± 7.1 Cd 0.23 ± 0.22 20.6 ± 9.7 0.01Pb – – –

T. albacares Yellowfin tuna 44 13.6 ± 17.2 86.2 ± 33.7 78.6 ± 30.2 Cd 0.18 ± 0.15 11.5 ± 9.8 0.01Pb 0.06 ± 0.04 0.041 ± 0.052 1.46

N, number of specimens; SD, standard deviation.a Crustaceans, fish and cephalopods.

100 J. Ruelas-Inzunza et al. / Marine Pollution Bulletin 87 (2014) 98–103

concentrations of Cd, Pb and 210Po in muscle tissue of the analyzedspecies and the prey that were found in the stomach contents wereused to estimate the transference factor (TF) according to Mackayand Fraser (2000): TF = Cc/Cp, where Cc represents the concentra-tion of the element of interest in the predator (consumer), and Cpis the concentration of the same element in the prey (whole stom-ach content). TF > 1 indicates that the metal is biomagnified (Gray,2002), and TF < 1 implies biodilution. Nitrogen isotopic ratios wereused to estimate the trophic position (TP) of tuna species by thefollowing equation (Post, 2002):

TP ¼ kþ ðd15Ntuna � d15Nbase of the food webÞ=k15N

where k is the trophic level of the base of the food web, d15N tuna isthe nitrogen signature of the fish of interest, and k15N is the trophicdiscrimination factor. In this study, we considered zooplankton asthe base of the food web (k = 2; d15Nbase = 10.63 ± 0.71‰) (Poppet al., 2007). To effectively apply isotopic values to study the metaltransfer in K. pelamis and T. albacares, we used an accurate labora-tory-based value of k15N of 1.9‰ measured in white muscle of T.orientalis (Madigan et al., 2012). Regression analyses were per-formed to establish the relationships between metal concentrations(Cd, Pb and 210Po) and the TP estimated for each specimen. A reci-procal or square root transformation of datasets was first performedto obtain normal distributions and homogeneous variances.

3. Results and discussion

From the biometric data of the collected tuna (Table 1), it can beobserved that the K. pelamis were adults; it has been documentedthat when this species reaches sexual maturity, the fork length isapproximately 45 cm (Collette, 1995). For T. albacares, weights ofthe specimens indicate (Schaefer, 1998) a mix of mature and juve-nile specimens.

Concentrations of Cd and Pb in muscle tissue and stomach con-tents and the corresponding transfer factors (TF) of the analyzedtuna are presented in Table 1. Stomach contents were composedof crustaceans, fish and cephalopods. Pb was not measured in K.pelamis. The mean concentrations of Cd in muscle from both tunaspecies were not significantly different (p > 0.05). Similarly, theCd levels in the stomach contents of K. pelamis and T. albacaresdid not differ significantly (p > 0.05). Regarding the TF of the ana-lyzed elements, the Pb values in T. albacares were above unity. Thisvalue indicates that this element is biomagnified during transfor-mation of the stomach contents into muscle in the yellowfin tuna.In some studies (Amiard et al., 1980; Szefer, 1991), it has been con-cluded that Cd and Pb are not biomagnified. In another study(Barwick and Maher, 2003) in a temperate estuarine ecosystem,the authors reported a positive transference of Cd and Pb, but onlyin some of the analyzed trophic interactions. In an experimentalfour-level food chain (Tetraselmis suecica-phytoplankton, Artemiafranciscana-brineshrimp, Litopenaeus vannamei-white shrimp,Haemulon scudderi-fish), it was found that Pb in phytoplanktonincreased with respect to the solution but decreased during succes-sive trophic transfers (Soto-Jiménez et al., 2011). In a study of the

trophic distribution of Cd and Pb from a subtropical lagoon in theGulf of California, Ruelas-Inzunza and Páez-Osuna (2008) foundthat the TFs of Cd were >1.0 in 64.5% of the examined trophic links;in the case of Pb, the TFs were >1 in only 45.2% of the trophic inter-actions. The concentrations of elements in prey and the approachused to estimate TF (homogenized stomach contents versus sepa-rate food items) can lead to contrasting conclusions about whetherbiomagnification is occurring. In addition, elemental bioavailabilitycan be influenced by environmental parameters, such as metal spe-ciation, mineralogy, pH, redox potential, temperature, and totalorganic content (Luoma, 1989).

The 210Po activity in the livers of T. albacares and K. pelamis ana-lyzed in our study and published information about the musclesand livers of multiple tuna species are presented in Table 2. Theaverage activity of 210Po was higher in the liver than in muscle.210Po activity in liver ranged from 119 Bq kg�1 in K. pelamis fromthe Eastern Pacific (this study) to 777 Bq kg�1 in T. albacaresfrom the Eastern Pacific (15�N; 100�W). In muscle, values rangedfrom 0.45 Bq kg�1 in T. albacares from the Eastern Pacific (from16 to 21�N) to 137 Bq kg�1 in T. thynnus from the MediterraneanSea (35�N). Clearly, the 210Po activity in muscle varied by severalorders of magnitude; inherent differences between the species oftuna or in their latitudes may explain this variance. In this context,Carvalho (2011) mentioned that 210Po activity in marine biota var-ies by several orders of magnitude and such variations are notrelated to water depth or geographical location.

With respect to the feeding behavior of the analyzed tuna,jumbo squid Dosidicus gigas and pelagic red crab Pleuroncodes plan-ipes are the main prey reported for T. albacares from the Easterntropical Pacific (Ordiano-Flores et al., 2012). Feeding habits of thesmallest individuals of tropical tuna are poorly known (Grahamet al., 2006). A study of small T. albacares found that specimenswith less than a 40 cm fork length (FL) fed on crustaceans, whilelarger specimens (>50 cm FL) used fish as food (Maldeniya,1996). d15N and d13C in the muscle of T. albacares and K. pelamisand the variation of d15N with tuna dimensions are presented inFig. 2. d13C values in T. albacares varied from �18.82 to�15.69‰; in K. pelamis they ranged from �18.2 to �16.32‰. Thewide variations in d13C indicate that organic matter is suppliedfrom diverse sources. For d15N, values ranged from 17.93 to12.24‰ in T. albacares and from 16.41 to 10.45‰ in K. pelamis.The variation of 15N values in marine predators can be due to dif-ferences in diet composition, the physiology of the individuals andthe nutrient dynamics at the base of the food web (Popp et al.,2007). A change in prey composition with age for tuna, frommainly crustaceans to a more varied diet composed of both fishand crustaceans, implies that an increase and a higher variabilityin d15N values is expected with age, especially in individuals witha larger than 45 cm FL (Bearhop et al., 2004). Trophic positions esti-mated for T. albacares averaged 4.60 ± 0.67 (2.85–5.84) and3.94 ± 1.06 (1.91–5.04) for K. pelamis. TP increased with FL for bothspecies (r P 0.89, p < 0.05). Based on diet data, Olson and Watters(2003) reported values of 4.66 and 4.57 for large yellowfin andskipjack from the Eastern tropical Pacific.

Table 2Comparison of 210Po activity (Bq kg�1 wet weight) in K. pelamis and T. albacares from the Eastern Pacific with other studies.

Species Common name Tissue 210Po Site Reference

T. albacares, T. obessus, T. alalunga,K. pelamisa

Yellowfin tuna, bigeye tuna, albacore,skipjack tuna

Muscle 5 Portugal coasts Carvalho (1988)

T. albacares, T. obessus, T. alalunga,K. pelamisa

Yellowfin tuna, bigeye tuna, albacore,skipjack tuna

Liver 288 Portugal coasts Carvalho (1988)

T. albacares Yellowfin tuna Muscle 0.45 Eastern Pacific Ruelas-Inzunza et al. (2012)K. pelamis Skipjack tuna Muscle 1.76 Eastern Pacific Ruelas-Inzunza et al. (2012)K. pelamis Skipjack tuna Muscle 18.5 Gulf of Panama Hoffman et al. (1974)K. pelamis Skipjack tuna Liver 407 Gulf of Panama Hoffman et al. (1974)T. albacares Yellowfin tuna Liver 777 15�N;100�W Hoffman et al. (1974)T. albacares Yellowfin tuna Muscle 14.8 15�N;100�W Hoffman et al. (1974)T. thynnus Bigeye tuna Muscle 137 Mediterranean Sea Heyraud and Cherry (1979)T. thynnus Bigeye tuna Liver 629 Mediterranean Sea Heyraud and Cherry (1979)T. obesus Bigeye tuna Muscle 3 Madeira Island (Portugal) Carvalho (2011)T. obesus Bigeye tuna Liver 268 Madeira Island (Portugal) Carvalho (2011)T. albacares Yellowfin tuna Liver 157 Eastern Pacific This studyK. pelamis Skipjack tuna Liver 119 Eastern Pacific This study

a Composite samples.

Fig. 2. Relation of d15N with d13C in muscle of Thunnus albacares and Katsuwonus pelamis (a); variation of d15N as a function of tuna dimensions (b–d).

J. Ruelas-Inzunza et al. / Marine Pollution Bulletin 87 (2014) 98–103 101

Variations of Cd and Pb (lg g�1 dry weight) and 210Po activity(Bq kg�1 dry weight) with TP of analyzed tuna species are includedin Fig. 3. The results revealed that Cd in muscle increased signifi-cantly with TP for K. pelamis (R2 = 0.24, F = 12.366, p = 0.0011)and for T. albacares (R2 = 0.19, F = 6.164, p = 0.0198), while Pbdecreased in T. albacares (R2 = 0.27, F = 11.79, p = 0.0017). Similarly,there was a significant trend of a decrease in 210Po in the liver of T.

albacares (R2 = 0.29, F = 5.01, p = 0.0449), excluding two outlier210Po values (Bq kg�1 dry weight) of 3145 and 3535.

The transfer of Pb from stomach contents to the muscle tissue ofT. albacares was positive (higher than one); this result implies thatthis element was biomagnified in the interaction between thewhole stomach content and the muscle tissue. As for 210Po activity,values in the liver of analyzed tuna were higher than in muscle of

Fig. 3. Variation of Cd and Pb concentrations (lg g�1 dry weight) and 210Po activity (Bq kg�1 dry weight) with trophic position of Katsuwonus pelamis and Thunnus albacares.

102 J. Ruelas-Inzunza et al. / Marine Pollution Bulletin 87 (2014) 98–103

the same species from different regions of the Eastern Pacific. d13Cin T. albacares and K. pelamis varied by 3.13 and 1.88‰, respec-tively, which indicates that organic matter sources are more variedin the yellowfin tuna T. albacares. d15N values in yellowfin tunawere higher than in skipjack tuna. Therefore, the trophic positionof T. albacares (4.60 ± 0.67) was more elevated than in K. pelamis(3.94 ± 1.06). In some cases, the analyzed elements increased inconcentration as a function of the trophic position; such behaviorwas observed for Cd in the muscle of both T. albacares and K.pelamis.

Acknowledgements

Financial support was partially provided by the Ministry of Pub-lic Education (Project REDES PROMEP/103.5/13/9335) and UNAM(project PAPIIT IN208813). Thanks are due to L.H. Pérez-Bernalfor the 210Po analysis and to G. Ramírez-Rezéndiz for computingassistance.

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